Fungal Taxonomy I:The Basal Fungi

The goal of modern taxonomy is to understand the relationships of living organisms in terms of evolutionary descent. If we say, for example, that two species are members of the same genus, then we are (or at least should be) saying that the two species are descended from a more recent common ancestor than one that they share with a species in another genus. The relationships between living organisms are understood in terms of nested clades - every time a speciation event takes place, two new clades are produced. If a species in that clade further evolves into two different species, two more clades are produced that are nested within the old clade. When a group of related clades are mapped together into a family tree-like arrangement, the tree is known as a phylogeny. The phylogeny of a particular group of organisms provides us with a diagrammatic outline of the evolutionary history of that group.

Ideally, all taxa (that is, taxonomic groupings) that are defined from such phylogenies should be monophyletic. A taxon is monophyletic when all of its members are part of the same clade, and all members of that clade are members of that taxon. If a subclade within the larger clade is not included in the taxon, that taxon is said to be paraphyletic. Since the phylogeny of all living organisms represents an infinitely nested series of clades, there are many instances in which taxa must be defined paraphyletically. However, a situation to be avoided is one in which a taxon is polyphyletic, that is, members of more than one single clade are grouped together in a common taxon.

Traditionally, taxa have been given Linnaean rank designations, ranging from kingdoms down to genera; however, since every speciation event produces a new clade, one rapidly runs out of Linnaean ranks to assign to them. Because of this, the concept of rank-free classification is taking hold, in which many newly discovered clades are not assigned a Linnaean rank at all. Linnaean ranks are still used, but mainly as placeholders to outline the system of biological classification.

Presently, we are in the midst of a period of great discovery and revision in our understanding of the taxonomy of all living organisms. Advances in molecular biological technique and computer-aided statistical analysis have allowed biologists to analyze genomes in much greater depth. Such analysis has confirmed many relationships that were inferred by morphological, anatomical, and physiological evidence, but has also falsified many long-held hypotheses about such relationships, and often revealed relationships that were not previously suspected.

About ten years ago, our understanding of fungal taxonomy had advanced to the point where it was understood that, based upon differences in cell structure and physiology, most of the groups that had been called "lower fungi" (cellular and plasmodial slime molds, oomycetes, hyphochytrids, etc.) were clearly not fungi at all, nor even closely related to fungi. The exception were the chytrids, which were thought to be a basal line in the Kingdom Fungi, having diverged from all other fungi very early in fungal evolution and retaining many of the "primitive" characteristics of the fungal ancestor.

It was also understood that fungi were more closely related to animals than they were to plants, algae, or any of the "lower fungi" (other than chytrids). The common ancestor of animals and fungi was thought to be a flagellate with similarities to the chytrids and the choanoflagellates (a group with great similarities to the hypothesized animal ancestor).

Figure 2 Phylogeny showing the major clades of the Kingdom Fungi. The group marked "OUTGROUPS" are non-fungi, and show the point where the phylogeny is rooted.

While recent findings have confirmed or refined many of these hypotheses, there have also been some surprising revisions. Most notably, it has been demonstrated that the Zygomycota are not a real monophyletic group, but instead represent a polyphyletic assemblage of parts of at least four different lineages, including a lineage that does not belong to the Kingdom Fungi at all.

Amoebidium, a trichomycete that grows in the guts of arthropods, has recently been found to belong to a group called the Mesomycetozoea, which are close relatives of the choanoflagellates. The mesomycetozoans and choanoflagellates together form a clade that diverged from the animal line at a point in animal evolution when the ancestors of animals had not yet strongly differentiated from the ancestors of fungi. It is very likely that further analysis will reveal many other trichomycetes to be mesomycetozoans rather than fungi.

The majority of taxa that were once classified as Zygomycota have been found to belong to a lineage consisting of the core zygomycetes plus the Blastocladiales, which used to be classified as chytrids. This clade occupies the basal position in the phylogeny of fungi, with molecular evidence showing that it diverged from the rest of the fungi at a very early point in fungal evolution. The next most basal clade consists of the chytrids (sans the Blastocladiales), plus several genera of former zygomycetes, including Endogone. (Endogone are an unusual group in that they are the only fungal taxon outside of the basidiomycetes and ascomycetes whose members are capable of forming ectomycorrhizae with plants.)

This new understanding of the basal phylogeny of fungi throws much of our prior understanding of fungal evolution into disarray. When the chytrids were thought to be the most basal clade in the fungi, the evolution of a predominantly hyphal fungal morphology from a zoosporic one was thought to have taken place only once. It now seems that this evolutionary event took place at least three times, or perhaps there may have been several shifts back and forth between predominantly zoosporic life histories and predominantly hyphal ones.

The remaining segregate clade of the zygomycetes consists of the VA mycorrhizal fungi and their relatives, a group that has recently been designated as the Phylum Glomeromycota. This group was found to be a basal member of the same clade as the Ascomycota and Basidiomycota. All glomeromycetes are either VA mycorrhiza-formers or live in mutualistic relationships with cyanobacteria. Interestingly, it appears that the diversification of the glomeromycetes roughly correlates with the time when plants are thought to have first colonized land, lending weight to the idea that these fungi played a role in this colonization.

So far, I have yet to discuss how the present revolution in fungal taxonomy has affected our understanding of the ascomycetes and basidiomycetes that we are so familiar with. This will be the topic of my next article.